Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase

Mallam, Anna L.; Sidote, David J.; Lambowitz, Alan M.

doi:10.7554/elife.04630

Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase

Journal Article · Fri Dec 12 00:00:00 EST 2014 · eLife

DOI:https://doi.org/10.7554/elife.04630· OSTI ID:1628825

Mallam, Anna L. ^[1]; Sidote, David J. ^[2]; Lambowitz, Alan M. ^[2]

Univ. of Texas, Austin, TX (United States); DOE/OSTI
Univ. of Texas, Austin, TX (United States)

How different helicase families with a conserved catalytic ‘helicase core’ evolved to function on varied RNA and DNA substrates by diverse mechanisms remains unclear. In this study, we used Mss116, a yeast DEAD-box protein that utilizes ATP to locally unwind dsRNA, to investigate helicase specificity and mechanism. Our results define the molecular basis for the substrate specificity of a DEAD-box protein. Additionally, they show that Mss116 has ambiguous substrate-binding properties and interacts with all four NTPs and both RNA and DNA. The efficiency of unwinding correlates with the stability of the ‘closed-state’ helicase core, a complex with nucleotide and nucleic acid that forms as duplexes are unwound. Crystal structures reveal that core stability is modulated by family-specific interactions that favor certain substrates. This suggests how present-day helicases diversified from an ancestral core with broad specificity by retaining core closure as a common catalytic mechanism while optimizing substrate-binding interactions for different cellular functions.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628825

Journal Information:: eLife, Journal Name: eLife Vol. 3; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (58)

Different conformations of double-stranded nucleic acid in solution as revealed by circular dichroism Ivanov, V. I.; Minchenkova, L. E.; Schyolkina, A. K. Biopolymers, Vol. 12, Issue 1 https://doi.org/10.1002/bip.1973.360120109	journal	January 1973
Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. Walker, J. E.; Saraste, M.; Runswick, M. J. The EMBO Journal, Vol. 1, Issue 8 https://doi.org/10.1002/j.1460-2075.1982.tb01276.x	journal	August 1982
Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase Tuteja, Narendra; Tarique, Mohammed; Banu, Mst. Sufara Akhter Plant Molecular Biology, Vol. 85, Issue 6 https://doi.org/10.1007/s11103-014-0209-6	journal	June 2014
X-Ray Structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase Core and Its Complex with DNA Dürr, Harald; Körner, Christian; Müller, Marisa Cell, Vol. 121, Issue 3 https://doi.org/10.1016/j.cell.2005.03.026	journal	May 2005
Unwinding by Local Strand Separation Is Critical for the Function of DEAD-Box Proteins as RNA Chaperones Del Campo, Mark; Mohr, Sabine; Jiang, Yue Journal of Molecular Biology, Vol. 389, Issue 4 https://doi.org/10.1016/j.jmb.2009.04.043	journal	June 2009
ATP-Dependent Roles of the DEAD-Box Protein Mss116p in Group II Intron Splicing In Vitro and In Vivo Potratz, Jeffrey P.; Del Campo, Mark; Wolf, Rachel Z. Journal of Molecular Biology, Vol. 411, Issue 3 https://doi.org/10.1016/j.jmb.2011.05.047	journal	August 2011
High-Throughput Genetic Identification of Functionally Important Regions of the Yeast DEAD-Box Protein Mss116p Mohr, Georg; Del Campo, Mark; Turner, Kathryn G. Journal of Molecular Biology, Vol. 413, Issue 5 https://doi.org/10.1016/j.jmb.2011.09.015	journal	November 2011
Structure of the Yeast DEAD Box Protein Mss116p Reveals Two Wedges that Crimp RNA Del Campo, Mark; Lambowitz, Alan M. Molecular Cell, Vol. 35, Issue 5 https://doi.org/10.1016/j.molcel.2009.07.032	journal	September 2009
SF1 and SF2 helicases: family matters Fairman-Williams, Margaret E.; Guenther, Ulf-Peter; Jankowsky, Eckhard Current Opinion in Structural Biology, Vol. 20, Issue 3 https://doi.org/10.1016/j.sbi.2010.03.011	journal	June 2010
Characterization of the NTPase, RNA-Binding, and RNA Helicase Activities of the DEAH-Box Splicing Factor Prp22 ^† Tanaka, Naoko; Schwer, Beate Biochemistry, Vol. 44, Issue 28 https://doi.org/10.1021/bi050407m	journal	July 2005
DEAD-Box Helicases Form Nucleotide-Dependent, Long-Lived Complexes with RNA Liu, Fei; Putnam, Andrea A.; Jankowsky, Eckhard Biochemistry, Vol. 53, Issue 2 https://doi.org/10.1021/bi401540q	journal	January 2014
Structural basis of RNA recognition and activation by innate immune receptor RIG-I Jiang, Fuguo; Ramanathan, Anand; Miller, Matthew T. Nature, Vol. 479, Issue 7373 https://doi.org/10.1038/nature10537	journal	September 2011
Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p Mallam, Anna L.; Del Campo, Mark; Gilman, Benjamin Nature, Vol. 490, Issue 7418 https://doi.org/10.1038/nature11402	journal	September 2012
From unwinding to clamping — the DEAD box RNA helicase family Linder, Patrick; Jankowsky, Eckhard Nature Reviews Molecular Cell Biology, Vol. 12, Issue 8 https://doi.org/10.1038/nrm3154	journal	July 2011
ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding Liu, F.; Putnam, A.; Jankowsky, E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 51 https://doi.org/10.1073/pnas.0811115106	journal	December 2008
Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail Mallam, A. L.; Jarmoskaite, I.; Tijerina, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 30 https://doi.org/10.1073/pnas.1109566108	journal	July 2011
An A-DNA triplet code: thermodynamic rules for predicting A- and B-DNA. Basham, B.; Schroth, G. P.; Ho, P. S. Proceedings of the National Academy of Sciences, Vol. 92, Issue 14 https://doi.org/10.1073/pnas.92.14.6464	journal	July 1995
A Steady-state and Pre-steady-state Kinetic Analysis of the NTPase Activity Associated with the Hepatitis C Virus NS3 Helicase Domain Preugschat, Frank; Averett, Devron R.; Clarke, Berwyn E. Journal of Biological Chemistry, Vol. 271, Issue 40 https://doi.org/10.1074/jbc.271.40.24449	journal	October 1996
IDT SciTools: a suite for analysis and design of nucleic acid oligomers Owczarzy, R.; Tataurov, A. V.; Wu, Y. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn198	journal	May 2008
Circular dichroism and conformational polymorphism of DNA Kypr, J.; Kejnovska, I.; Renciuk, D. Nucleic Acids Research, Vol. 37, Issue 6 https://doi.org/10.1093/nar/gkp026	journal	January 2009
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/s0021889807021206	journal	July 2007
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Cytosolic Viral Sensor RIG-I Is a 5'-Triphosphate-Dependent Translocase on Double-Stranded RNA Myong, S.; Cui, S.; Cornish, P. V. Science, Vol. 323, Issue 5917 https://doi.org/10.1126/science.1168352	journal	February 2009
The anatomy of A-, B-, and Z-DNA Dickerson, R.; Drew, H.; Conner, B. Science, Vol. 216, Issue 4545 https://doi.org/10.1126/science.7071593	journal	April 1982
Enzyme Promiscuity: A Mechanistic and Evolutionary Perspective Khersonsky, Olga; Tawfik, Dan S. Annual Review of Biochemistry, Vol. 79, Issue 1, p. 471-505 https://doi.org/10.1146/annurev-biochem-030409-143718	journal	June 2010
Structure and Mechanism of Helicases and Nucleic Acid Translocases Singleton, Martin R.; Dillingham, Mark S.; Wigley, Dale B. Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.76.052305.115300	journal	June 2007
Enzyme Recruitment in Evolution of New Function Jensen, R. A. Annual Review of Microbiology, Vol. 30, Issue 1 https://doi.org/10.1146/annurev.mi.30.100176.002205	journal	October 1976
Mechanism of Mss116 ATPase reveals functional diversity of DEAD-Box proteins. Cao, Wenxiang; Coman, Maria Magdalena; Ding, Steve Figshare https://doi.org/10.1184/r1/6103718	text	January 2018
Comparative Structural Analysis of Human DEAD-Box RNA Helicases Schütz, Patrick; Karlberg, Tobias; van den Berg, Susanne PLoS ONE, Vol. 5, Issue 9 https://doi.org/10.1371/journal.pone.0012791	journal	September 2010
Arabidopsis DEAD-box RNA helicase UAP56 interacts with both RNA and DNA as well as with mRNA export factors Kammel, Christine; Thomaier, Maren; Sørensen, Brian B. Universität Regensburg https://doi.org/10.5283/epub.28787	text	January 2013
DEAD-box proteins as RNA helicases and chaperones: DEAD-box proteins Jarmoskaite, Inga; Russell, Rick Wiley Interdisciplinary Reviews: RNA, Vol. 2, Issue 1 https://doi.org/10.1002/wrna.50	journal	September 2010
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Molecular structure of a complete turn of A-DNA Verdaguer, Nuria; Aymamí, Joan; Fernández-Forner, Dolors Journal of Molecular Biology, Vol. 221, Issue 2 https://doi.org/10.1016/0022-2836(91)80077-8	journal	September 1991
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Helicases: amino acid sequence comparisons and structure-function relationships Gorbalenya, Alexander E.; Koonin, Eugene V. Current Opinion in Structural Biology, Vol. 3, Issue 3 https://doi.org/10.1016/S0959-440X(05)80116-2	journal	June 1993
Structural Basis of RNA Recognition and Activation by Innate Immune Receptor RIG-I Ramanathan, Anand; Jiang, Fuguo; Miller, Matthew T. Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.11.3273	journal	January 2012
Crystal Structure and Nucleotide Binding of the Thermus thermophilus RNA Helicase Hera N-terminal Domain Rudolph, Markus G.; Heissmann, Ramona; Wittmann, Julia G. Journal of Molecular Biology, Vol. 361, Issue 4 https://doi.org/10.1016/j.jmb.2006.06.065	journal	August 2006
Involvement of DEAD-box Proteins in Group I and Group II Intron Splicing. Biochemical Characterization of Mss116p, ATP Hydrolysis-dependent and -independent Mechanisms, and General RNA Chaperone Activity Halls, Coralie; Mohr, Sabine; Del Campo, Mark Journal of Molecular Biology, Vol. 365, Issue 3 https://doi.org/10.1016/j.jmb.2006.09.083	journal	January 2007
Function of the C-terminal Domain of the DEAD-box Protein Mss116p Analyzed in Vivo and in Vitro Mohr, Georg; Del Campo, Mark; Mohr, Sabine Journal of Molecular Biology, Vol. 375, Issue 5 https://doi.org/10.1016/j.jmb.2007.11.041	journal	February 2008
Mechanism of Mss116 ATPase Reveals Functional Diversity of DEAD-Box Proteins Cao, Wenxiang; Coman, Maria Magdalena; Ding, Steve Journal of Molecular Biology, Vol. 409, Issue 3 https://doi.org/10.1016/j.jmb.2011.04.004	journal	June 2011
DEAD-Box Proteins Unwind Duplexes by Local Strand Separation Yang, Quansheng; Del Campo, Mark; Lambowitz, Alan M. Molecular Cell, Vol. 28, Issue 2 https://doi.org/10.1016/j.molcel.2007.08.016	journal	October 2007
Parts, assembly and operation of the RIG-I family of motors Rawling, David C.; Pyle, Anna Marie Current Opinion in Structural Biology, Vol. 25 https://doi.org/10.1016/j.sbi.2013.11.011	journal	April 2014
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function Huang, H. -R.; Rowe, C. E.; Mohr, S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 1 https://doi.org/10.1073/pnas.0407896101	journal	December 2004
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA Henn, A.; Cao, W.; Licciardello, N. Proceedings of the National Academy of Sciences, Vol. 107, Issue 9 https://doi.org/10.1073/pnas.0913081107	journal	February 2010
Cofactor-dependent specificity of a DEAD-box protein Young, C. L.; Khoshnevis, S.; Karbstein, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 29 https://doi.org/10.1073/pnas.1302577110	journal	April 2013
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
RNA Helicase Proteins as Chaperones and Remodelers Jarmoskaite, Inga; Russell, Rick Annual Review of Biochemistry, Vol. 83, Issue 1 https://doi.org/10.1146/annurev-biochem-060713-035546	journal	June 2014
Translocation and Unwinding Mechanisms of RNA and DNA Helicases Pyle, Anna Marie Annual Review of Biophysics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.biophys.37.032807.125908	journal	June 2008
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA. Henn, Arnon; Cao, Wenxiang; Licciardello, Nicholas Carnegie Mellon University https://doi.org/10.1184/r1/6103988	text	January 2010
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA. Henn, Arnon; Cao, Wenxiang; Licciardello, Nicholas Carnegie Mellon University https://doi.org/10.1184/r1/6103988.v1	text	January 2010
Arabidopsis DEAD-Box RNA Helicase UAP56 Interacts with Both RNA and DNA as well as with mRNA Export Factors Kammel, Christine; Thomaier, Maren; Sørensen, Brian B. PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0060644	journal	March 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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